TRIM5α and species tropism of HIV/SIV

Frontiers in Microbiology

Volumn 3, Issue JAN, 2012, Pages

  Nakayama, Emi E ^a   Shioda, Tatsuo ^a  

^a OSAKA UNIVERSITY   (Japan)

Author keywords

Cynomolgus monkey; Hiv 1; HIV 2; Rhesus monkey; SIV; TRIM5 ; TRIMCyp

Indexed keywords

EID: 84868102045     PISSN: None     EISSN: 1664302X     Source Type: Journal    
DOI: 10.3389/fmicb.2012.00013     Document Type: Article

References (135)

1. Akari, H., Mori, K., Terao, K., Otani, I., Fukasawa, M., Mukai, R., and Yoshikawa, Y. (1996). In vitro immortalization of old world monkey T lymphocytes with Herpesvirus saimiri: its susceptibility to infection with simian immunodeficiency viruses. Virology 218, 382-388.
2. Akari, H., Nam, K. H., Mori, K., Otani, I., Shibata, H., Adachi, A., Terao, K., and Yoshikawa, Y. (1999). Effects of SIVmac infection on peripheral blood CD4+CD8+ T lymphocytes in cynomolgus macaques. Clin. Immunol. 91, 321-329.
3. Alkhatib, G., Combadiere, C., Broder, C. C., Feng, Y., Kennedy, P. E., Murphy, P. M., and Berger, E. A. (1996). CC CKR5: a RANTES, MIP-1alpha, MIP-1beta receptor as a fusion cofactor for macrophage-tropic HIV-1. Science 272,1955-1958.
4. Anderson, J. L., Campbell, E. M., Wu, X., Vandegraaff, N., Engelman, A., and Hope, T. J. (2006). Proteasome inhibition reveals that a functional preintegration complex intermediate can be generated during restriction by diverse TRIM5 proteins. J. Virol. 80, 9754-9760.
5. Berthoux, L., Sebastian, S., Sayah, D. M., and Luban, J. (2005). Disruption of human TRIM5alpha antiviral activity by nonhuman primate orthologues. J. Virol. 79, 7883-7888.
6. Berthoux, L., Sebastian, S., Sokolskaja, E., and Luban, J. (2004). Lv1 inhibition of human immunodeficiency virus type 1 is counteracted by factors that stimulate synthesis or nuclear translocation of viral cDNA. J. Virol. 78, 11739-11750.
7. Bieniasz, P. D., and Cullen, B. R. (2000). Multiple blocks to human immunodeficiency virus type 1 replication in rodent cells. J. Virol. 74, 9868-9877.
8. Bieniasz, P. D., Fridell, R. A., Anthony, K., and Cullen, B. R. (1997). Murine CXCR-4 is a functional corecep-tor for T-cell-tropic and dual-tropic strains of human immunodeficiency virus type 1. J. Virol. 71, 7097-7100.
9. Bleul, C. C., Farzan, M., Choe, H., Parolin, C., Clark-Lewis, I., Sodroski, J., and Springer, T. A. (1996). The lymphocyte chemoattractant SDF-1 is a ligand for LESTR/fusin and blocks HIV-1 entry. Nature 382, 829-833.
10. Brass, A. L., Dykxhoorn, D. M., Benita, Y., Yan, N., Engelman, A., Xavier, R. J., Lieberman, J., and Elledge, S. J. (2008). Identification of host proteins required for HIV infection through a functional genomic screen. Science 319, 921-926.
11. Brennan, G., Kozyrev, Y., and Hu, S. L. (2008). TRIMCyp expression in Old World primates Macaca nemestrina and Macaca fascicularis. Proc. Natl. Acad. Sci. U.S.A. 105, 3569-3574.
12. Brennan, G., Kozyrev, Y., Kodama, T., and Hu, S. L. (2007). Novel TRIM5 isoforms expressed by Macaca nemestrina. J. Virol. 81, 12210-12217.
13. Browning, J., Horner, J. W., Pettoello-Mantovani, M., Raker, C., Yurasov, S., Depinho, R. A., and Goldstein, H. (1997). Mice transgenic for human CD4 and CCR5 are susceptible to HIV infection. Proc. Natl. Acad. Sci. U.S.A. 94, 14637-14641.
14. Castro, B. A., Barnett, S. W., Evans, L. A., Moreau, J., Odehouri, K., and Levy, J. A. (1990). Biologic heterogeneity of human immunodeficiency virus type 2 (HIV-2) strains. Virology 178, 527-534.
15. Castro, B. A., Nepomuceno, M., Lerche, N. W., Eichberg, J. W., and Levy, J. A. (1991). Persistent infection of baboons and rhesus monkeys with different strains of HIV-2. Virology 184,219-226.
16. Chackerian, B., Long, E. M., Luciw, P. A., and Overbaugh, J. (1997). Human immunodeficiency virus type 1 core-ceptors participate in postentry stages in the virus replication cycle and function in simian immunodeficiency virus infection. J. Virol. 71, 3932-3939.
17. Cherepanov, P., Maertens, G., Proost, P., Devreese, B., Van Beeumen, J., Engelborghs, Y., De Clercq, E., and Debyser, Z. (2003). HIV-1 integrase forms stable tetramers and associates with LEDGF/p75 protein in human cells. J. Biol. Chem. 278, 372-381.
18. Choe, H., Farzan, M., Sun, Y., Sullivan, N., Rollins, B., Ponath, P. D., Wu, L., Mackay, C. R., Larosa, G., Newman, W., Gerard, N., Gerard, C., and Sodroski, J. (1996). The beta-chemokine receptors CCR3 and CCR5 facilitate infection by primary HIV-1 isolates. Cell 85, 1135-1148.
19. Christ, F., Thys, W., De Rijck, J., Gijs-bers, R., Albanese, A., Arosio, D., Emiliani, S., Rain, J. C., Benarous, R., Cereseto, A., and Debyser, Z. (2008). Transportin-SR2 imports HIV into the nucleus. Curr. Biol. 18, 1192-1202.
20. Cullen, B. R. (1991). Regulation of HIV-1 gene expression. FASEB J. 5, 2361-2368.
21. Daniel, M. D., Letvin, N. L., King, N. W., Kannagi, M., Sehgal, P. K., Hunt, R. D., Kanki, P. J., Essex, M., and Desrosiers, R. C. (1985). Isolation of T-cell tropic HTLV-III-like retro-virus from macaques. Science 228, 1201-1204.
22. Deng, H., Liu, R., Ellmeier, W., Choe, S., Unutmaz, D., Burkhart, M., Di Marzio, P., Marmon, S., Sutton, R. E., Hill, C. M., Davis, C. B., Peiper, S. C., Schall, T. J., Littman, D. R., and Landau, N. R. (1996). Identification of a major co-receptor for primary isolates of HIV-1. Nature 381,661-666.
23. Diaz-Griffero, F., Qin, X. R., Hayashi, F., Kigawa, T., Finzi, A., Sarnak, Z., Lien-laf, M., Yokoyama, S., and Sodroski, J. (2009). A B-box 2 surface patch important for TRIM5alpha self-association, capsid-binding avidity and retrovirus restriction. J. Virol. 83, 10737-10751.
24. Dietrich, E. A., Brennan, G., Ferguson, B., Wiseman, R. W., O'Connor, D., and Hu, S. L. (2011). Variable prevalence and functional diversity of the antiretroviral restriction factor TRIMCyp in Macaca fascicularis. J. Virol. 85, 9956-9963.
25. Doranz, B. J., Rucker, J., Yi, Y., Smyth, R. J., Samson, M., Peiper, S. C., Parmen-tier, M., Collman, R. G., and Doms, R. W (1996). A dual-tropic primary HIV-1 isolate that uses fusin and the beta-chemokine receptors CKR-5, CKR-3, and CKR-2b as fusion cofactors. Cell 85, 1149-1158.
26. Dragic, T., Litwin, V., Allaway, G. P., Martin, S. R., Huang, Y., Nagashima, K. A., Cayanan, C., Maddon, P. J., Koup, R. A., Moore, J. P., and Paxton, W. A. (1996). HIV-1 entry into CD4+ cells is mediated by the chemokine receptor CC-CKR-5. Nature 381, 667-673.
27. Feinberg, M. B., Baltimore, D., and Frankel, A. D. (1991). The role of Tat in the human immunodeficiency virus life cycle indicates a primary effect on transcriptional elongation. Proc. Natl. Acad. Sci. U.S.A. 88, 4045-4049.
28. Feinberg, M. B., Jarrett, R. F., Aldovini, A., Gallo, R. C., and Wong-Staal, F. (1986). HTLV-III expression and production involve complex regulation at the levels of splicing and translation of viral RNA. Cell 46, 807-817.
29. Feng, Y., Broder, C. C., Kennedy, P. E., and Berger, E. A. (1996). HIV-1 entry cofactor: functional cDNA cloning of a seven-transmembrane, G protein-coupled receptor. Science 272, 872-877.
30. Fenizia, C., Keele, B. F., Nichols, D., Cornara, S., Binello, N., Vaccari, M., Pegu, P., Robert-Guroff, M., Ma, Z. M., Miller, C. J., Ven-zon, D., Hirsch, V., and Fran-chini, G. (2011). TRIM5alpha does not affect simian immunodeficiency virus SIV(mac251) replication in vaccinated or unvaccinated Indian rhesus macaques following intrarec-tal challenge exposure. J. Virol. 85, 12399-12409.
31. Fujita, M., Yoshida, A., Sakurai, A., Tatsuki, J., Ueno, F., Akari, H., andAdachi,A. (2003). Susceptibility of HVS-immortalized lymphocytic HSC-F cells to various strains and mutants of HIV/SIV. Int.J. Mol. Med. 11,641-644.
32. Ganser-Pornillos, B. K., Chan-drasekaran, V., Pornillos, O., Sodroski, J. G., Sundquist, W I., and Yeager, M. (2011). Hexagonal assembly of a restricting TRIM5alpha protein. Proc. Natl. Acad. Sci. U.S.A. 108, 534-539.
33. Gao, F., Bailes, E., Robertson, D. L., Chen, Y., Rodenburg, C. M., Michael, S. F., Cummins, L. B., Arthur, L. O., Peeters, M., Shaw, G. M., Sharp, P. M., and Hahn, B. H. (1999). Origin of HIV-1 in the chimpanzee Pan troglodytes troglodytes. Nature 397, 436-441.
34. Garber, M. E., and Jones, K. A. (1999). HIV-1 Tat: coping with negative elongation factors. Curr. Opin. Immunol. 11,460-465.
35. Garber, M. E., Wei, P., Kewalramani, V N., Mayall, T. P., Herrmann, C. H., Rice, A. P., Littman, D. R., and Jones, K. A. (1998). The interaction between HIV-1 Tat and human cyclin T1 requires zinc and a critical cysteine residue that is not conserved in the murine CycT1 protein. Genes Dev. 12,3512-3527.
36. Gupta, R. K., Mlcochova, P., Pelchen-Matthews, A., Petit, S. J., Mat-tiuzzo, G., Pillay, D., Takeuchi, Y., Marsh, M., and Towers, G. J. (2009). Simian immunodeficiency virus envelope glycoprotein counteracts tetherin/BST-2/CD317 by intra-cellular sequestration. Proc. Natl. Acad.Sci. U.S.A. 106,20889-20894.
37. Hahn, B. H., Shaw, G. M., De Cock, K. M., and Sharp, P. M. (2000). AIDS as a zoonosis: scientific and public health implications. Science 287, 607-614.
38. Harris, R. S., Bishop, K. N., Sheehy, A. M., Craig, H. M., Petersen-Mahrt, S. K., Watt, I. N., Neuberger, M. S., and Malim, M. H. (2003). DNA deamination mediates innate immunity to retroviral infection. Cell 113, 803-809.
39. Hatziioannou, T., Ambrose, Z., Chung, N. P., Piatak, M. Jr., Yuan, F., Trubey, C. M., Coalter, V., Kiser, R., Schneider, D., Smedley, J., Pung, R., Gathuka, M., Estes, J. D., Veazey, R. S., Kewalramani, V. N., Lifson, J. D., and Bieniasz, P. D. (2009). A macaque model of HIV-1 infection. Proc. Natl. Acad. Sci U.S.A. 106, 4425-4429.
40. Hatziioannou, T., Perez-Caballero, D., Yang, A., Cowan, S., and Bieniasz, P. D. (2004). Retrovirus resistance factors Ref 1 and Lv1 are species-specific variants of TRIM5alpha. Proc. Natl. Acad. Sci. U.S.A. 101, 10774-10779.
41. Hatziioannou, T., Princiotta, M., Piatak, M. Jr., Yuan, F., Zhang, F., Lifson, J. D., and Bieniasz, P. D. (2006). Generation of simian-tropic HIV-1 by restriction factor evasion. Science 314,95.
42. Himathongkham, S., and Luciw, P. A. (1996). Restriction of HIV-1 (subtype B) replication at the entry step in rhesus macaque cells. Virology 219,485-488.
43. Hirsch, V., Adger-Johnson, D., Campbell, B., Goldstein, S., Brown, C., Elkins, W. R., and Monte-fiori, D. C. (1997). A molecularly cloned, pathogenic, neutralization-resistant simian immunodeficiency virus, SIVsmE543-3. J. Virol. 71, 1608-1620.
44. Igarashi, T., Iyengar, R., Byrum, R. A., Buckler-White, A., Dewar, R. L., Buckler, C. E., Lane, H. C., Kamada, K., Adachi, A., and Martin, M. A. (2007). Human immunodeficiency virus type 1 derivative with 7% simian immunodeficiency virus genetic content is able to establish infections in pig-tailed macaques. J. Virol. 81,11549-11552.
45. Jackson, P. K., Eldridge, A. G., Freed, E., Furstenthal, L., Hsu, J. Y., Kaiser, B. K., and Reimann, J. D. (2000). The lore of the RINGs: substrate recognition and catalysis by ubiq-uitin ligases. Trends Cell Biol. 10, 429-439.
46. Javanbakht, H., Diaz-Griffero, F., Strem-lau, M., Si, Z., and Sodroski, J. (2005). The contribution of RING and B-box 2 domains to retroviral restriction mediated by monkey TRIM5alpha. J. Biol. Chem. 280, 26933-26940.
47. Javanbakht, H., Yuan, W., Yeung, D. F., Song, B., Diaz-Griffero, F., Li, Y., Li, X., Stremlau, M., and Sodroski, J. (2006). Characterization of TRIM5alpha trimerization and its contribution to human immunode ficiency virus capsid binding. Virology 353, 234-246.
48. Jia, B., Serra-Moreno, R., Neidermyer, W., Rahmberg, A., Mackey, J., Fofana, I. B., Johnson, W E., Westmoreland, S., and Evans, D. T. (2009). Species-specific activity of SIV Nef and HIV-1 Vpu in overcoming restriction by tetherin/BST2. PLoS Pathog. 5, e1000429. doi:10.1371/journal.ppat.1000429
49. Joag, S. V., Li, Z., Foresman, L., Stephens, E. B., Zhao, L. J., Adany, I., Pinson, D. M., Mcclure, H. M., and Narayan, O. (1996). Chimeric simian/human immunodeficiency virus that causes progressive loss of CD4+ T cells and AIDS in pig-tailed macaques. J. Virol. 70, 3189-3197.
50. Jones, K. A., Kadonaga, J. T., Luciw, P. A., and Tjian, R. (1986). Activation of the AIDS retrovirus promoter by the cellular transcription factor, Sp1. Science 232, 755-759.
51. Kaiser, S. M., Malik, H. S., and Emer-man, M. (2007). Restriction of an extinct retrovirus by the human TRIM5alpha antiviral protein. Science 316, 1756-1758.
52. Kamada, K., Igarashi, T., Martin, M. A., Khamsri, B., Hatcho, K., Yamashita, T., Fujita, M., Uchiyama, T., and Adachi, A. (2006). Generation of HIV-1 derivatives that productively infect macaque monkey lymphoid cells. Proc. Natl. Acad. Sci. U.S.A. 103, 16959-16964.
53. Kar, A. K., Diaz-Griffero, F., Li, Y., Li, X., and Sodroski, J. (2008). Biochemical and biophysical characterization of a chimeric TRIM21-TRIM5alpha protein. J. Virol. 82,11669-11681.
54. Keppler, O. T., Yonemoto, W., Welte, E J., Patton, K. S., Iacovides, D., Atchison, R. E., Ngo, T., Hirschberg, D. L., Speck, R. F., and Goldsmith, M. A. (2001). Susceptibility of rat-derived cells to replication by human immunodeficiency virus type 1. J. Virol. 75, 8063-8073.
55. Kim, J., Tipper, C., and Sodroski, J. (2011). Role of TRIM5alpha RING domain E3 ubiquitin ligase activity in capsid disassembly, reverse transcription blockade, and restriction of simian immunodeficiency virus. J. Virol. 85, 8116-8132.
56. Kirmaier, A., Wu, F., Newman, R. M., Hall, L. R., Morgan, J. S., O'Connor, S., Marx, P. A., Meythaler, M., Goldstein, S., Buckler-White, A., Kaur, A., Hirsch, V M., and Johnson, W E. (2010). TRIM5 suppresses cross-species transmission of a primate immunodeficiency virus and selects for emergence of resistant variants in the new species. PLoS Biol. 8, e1000462. doi:10.1371/jour-nal.pbio.1000462
57. Koito, A., Kameyama, Y., Cheng-Mayer, C., and Matsushita, S. (2003a). Susceptibility of mink (Mustera vision)-derived cells to replication by human immunodeficiency virus type 1. J. Virol. 77,5109-5117.
58. Koito, A., Shigekane, H., and Matsushita, S. (2003b). Ability of small animal cells to support the postin-tegration phase of human immunodeficiency virus type-1 replication. Virology 305, 181-191.
59. Kono, K., Bozek, K., Domingues, E S., Shioda, T., and Nakayama, E. E. (2009). Impact of a single amino acid in the variable region 2 of the Old World monkey TRIM5alpha SPRY (B30.2) domain on anti-human immunodeficiency virus type 2 activity. Virology 388, 160-168.
60. Kono, K., Song, H., Shingai, Y., Shioda, T., and Nakayama, E. E. (2008). Comparison of anti-viral activity of rhesus monkey and cynomolgus monkey TRIM5alphas against human immunodeficiency virus type 2 infection. Virology 373, 447-456.
61. Kono, K., Song, H., Yokoyama, M., Sato, H., Shioda, T., and Nakayama, E. E. (2010). Multiple sites in the N-terminal half of simian immunodeficiency virus capsid protein contribute to evasion from rhesus monkey TRIM5alpha-mediated restriction. Retrovirology 7, 72.
62. Kootstra, N. A., Munk, C., Tonnu, N., Landau, N. R., and Verma, I. M. (2003). Abrogation of postentry restriction of HIV-1-based lentiviral vector transduction in simian cells. Proc. Natl. Acad. Sci. U.S.A. 100, 1298-1303.
63. Kuroishi, A., Bozek, K., Shioda, T., and Nakayama, E. E. (2010). A single amino acid substitution of the human immunodeficiency virus type 1 capsid protein affects viral sensitivity to TRIM5 alpha. Retrovirology 7, 58.
64. Kuroishi, A., Saito, A., Shingai, Y., Shioda, T., Nomaguchi, M., Adachi, A., Akari, H., and Nakayama, E. E. (2009). Modification of a loop sequence between alpha-helices 6 and 7 of virus capsid (CA) protein in a human immunodeficiency virus type 1 (HIV-1) derivative that has simian immunodeficiency virus (SIVmac239) vif and CA alpha-helices 4 and 5 loop improves replication in cynomolgus monkey cells. Retrovirology 6, 70.
65. LaBonte, J. A., Babcock, G. J., Patel, T., and Sodroski, J. (2002). Blockade of HIV-1 infection of newworld monkey cells occurs primarily at the stage of virus entry. J. Exp. Med. 196, 431-445.
66. Laguette, N., Sobhian, B., Casartelli, N., Ringeard, M., Chable-Bessia, C., Segeral, E., Yatim, A., Emiliani, S., Schwartz, O., and Benkirane, M. (2011). SAMHD1 is the dendritic- and myeloid-cell-specific HIV-1 restriction factor counteracted by Vpx. Nature 474, 654-657.
67. Landau, N. R., Warton, M., and Littman, D. R. (1988). The envelope glycoprotein of the human immunodeficiency virus binds to the immunoglobulin-like domain of CD4. Nature 334, 159-162.
68. Langelier, C. R., Sandrin, V., Eckert, D. M., Christensen, D. E., Chandrasekaran, V., Alam, S. L., Aiken, C., Olsen, J. C., Kar, A. K., Sodroski, J. G., and Sundquist, W. I. (2008). Biochemical characterization of a recombinant TRIM5alpha protein that restricts human immunodeficiency virus type 1 replication. J. Virol. 82, 11682-11694.
69. Laspia, M. F., Rice, A. P., and Mathews, M. B. (1989). HIV-1 Tat protein increases transcriptional initiation and stabilizes elongation. Cell 59,283-292.
70. Li, X., and Sodroski, J. (2008). The TRIM5alpha B-box 2 domain promotes cooperative binding to the retroviral capsid by mediating higher-order self-association. J. Virol. 82, 11495-11502.
71. Liao, C. H., Kuang, Y Q., Liu, H. L., Zheng, Y T., and Su, B. (2007). A novel fusion gene, TRIM5-cyclophilin A in the pig-tailed macaque determines its susceptibility to HIV-1 infection. AIDS 21(Suppl. 8),S19-S26.
72. Lim, S. Y., Chan, T., Gelman, R. S., Whitney, J. B., O'Brien, K. L., Barouch, D. H., Goldstein, D. B., Haynes, B. E, and Letvin, N. L. (2010a). Con tributions of Mamu-A*01 status and TRIM5 allele expression, but not CCL3L copy number variation, to the control of SIVmac251 replication in Indian-origin rhesus monkeys. PLoS Genet. 6, e1000997. doi:10.1371/journal.pgen.1000997
73. Lim, S. Y., Rogers, T., Chan, T., Whitney, J. B., Kim, J., Sodroski, J., and Letvin, N. L. (2010b). TRIM5alpha modulates immunodeficiency virus control in rhesus monkeys. PLoS Pathog. 6, e1000738. doi:10.1371/journal.ppat.1000738
74. Lin, T. Y., and Emerman, M. (2008). Determinants of cyclophilin A-dependent TRIM5 alpha restriction against HIV-1. Virology 379, 335-341.
75. Locher, C. P., Blackbourn, D. J., Herndier, B. G., Reyes-Teran, G., Barnett, S. W., Murthy, K. K., and Levy, J. A. (1998). Transient virus infection and pathogenesis of a new HIV type 2 isolate, UC12, in baboons. AIDS Res. Hum. Retroviruses 14, 79-82.
76. Locher, C. P., Witt, S. A., Herndier, B. G., Abbey, N. W., Tenner'Racz, K., Racz, P., Kiviat, N. B., Murthy, K. K., Brasky, K., Leland, M., and Levy, J. A. (2003). Increased virus replication and virulence after serial passage of human immunodeficiency virus type 2 in baboons. J. Virol. 77, 77-83.
77. Lores, P., Boucher, V., Mackay, C., Pla, M., Von Boehmer, H., Jami, J., Barre-Sinoussi, F., and Weill, J. C. (1992). Expression of human CD4 in transgenic mice does not confer sensitivity to human immunodeficiency virus infection. AIDS Res. Hum. Retroviruses 8, 2063-2071.
78. Maegawa, H., Miyamoto, T., Sakuragi, J., Shioda, T., and Nakayama, E. E. (2010). Contribution of RING domain to retrovirus restriction by TRIM5alpha depends on combination of host and virus. Virology 399, 212-220.
79. Maertens, G., Cherepanov, P., Pluymers, W., Busschots, K., De Clercq, E., Debyser, Z., and Engelborghs, Y. (2003). LEDGF/p75 is essential for nuclear and chromosomal targeting of HIV-1 integrase in human cells. J. Biol. Chem. 278, 33528-33539.
80. Mancebo, H. S., Lee, G., Flygare, J., Tomassini, J., Luu, P., Zhu, Y., Peng, J., Blau, C., Hazuda, D., Price, D., and Flores, O. (1997). P-TEFb kinase is required for HIV Tat transcriptional activation in vivo and in vitro. Genes Dev. 11,2633-2644.
81. Mangeat, B., Turelli, P., Caron, G., Friedli, M., Perrin, L., and Trono, D. (2003). Broad antiretroviral defence by human APOBEC3G through lethal editing of nascent reverse transcripts. Nature 424, 99-103.
82. Mariani, R., Chen, D., Schrofelbauer, B., Navarro, F., Konig, R., Bollman, B., Munk, C., Nymark-Mcmahon, H., and Landau, N. R. (2003). Species-specific exclusion of APOBEC3G from HIV-1 virions by Vif. Cell 114, 21-31.
83. Mariani, R., Rutter, G., Harris, M. E., Hope, T. J., Krausslich, H. G., and Landau, N. R. (2000). A block to human immunodeficiency virus type 1 assembly in murine cells. J. Virol. 74, 3859-3870.
84. Marin, M., Rose, K. M., Kozak, S. L., and Kabat, D. (2003). HIV-1 Vif protein binds the editing enzyme APOBEC3G and induces its degradation. Nat. Med. 9, 1398-1403.
85. Mische, C. C., Javanbakht, H., Song, B., Diaz-Griffero, F., Stremlau, M., Strack, B., Si, Z., and Sodroski, J. (2005). Retroviral restriction factor TRIM5alpha is a trimer. J. Virol. 79, 14446-14450.
86. Miyamoto, T., Yokoyama, M., Kono, K., Shioda, T., Sato, H., and Nakayama, E. E. (2011). A single amino acid of human immunodeficiency virus type 2 capsid protein affects conformation of two external loops and viral sensitivity to TRIM5alpha. PLoS ONE 6, e22779. doi:10.1371/journal.pone.0022779
87. Munk, C., Brandt, S. M., Lucero, G., and Landau, N. R. (2002). A dominant block to HIV-1 replication at reverse transcription in simian cells. Proc. Natl. Acad. Sci. U.S.A. 99, 13843-13848.
88. Nagai-Fukataki, M., Ohashi, T., Hashimoto, I., Kimura, T., Hakata, Y., and Shida, H. (2011). Nuclear and cytoplasmic effects of human CRM1 on HIV-1 production in rat cells. Genes Cells 16, 203-216.
89. Nakayama, E. E., Maegawa, H., and Shioda, T. (2006). A dominant-negative effect of cynomolgus monkey tripartite motif protein TRIM5alpha on anti-simian immunodeficiency virus SIVmac activity of an African green monkey orthologue. Virology 350, 158-163.
90. Nakayama, E. E., Miyoshi, H., Nagai, Y., and Shioda, T. (2005). A specific region of 37 amino acid residues in the SPRY (B30.2) domain of African green monkey TRIM5alpha determines species-specific restriction of simian immunodeficiency virus SIVmac infection. J. Virol. 79, 8870-8877.
91. Nakayama, E. E., Shingai, Y., Kono, K., and Shioda, T. (2008). TRIM5 alpha-independent anti-human immunodeficiency virus type 1 activity mediated by cyclophilin A in old world monkey cells. Virology 375,514-520.
92. Nakayama, E. E., and Shioda, T. (2010). Anti-retroviral activity of TRIM5 alpha. Rev. Med. Virol. 20, 77-92.
93. Neil, S. J., Zang, T., and Bieniasz, P. D. (2008). Tetherin inhibits retrovirus release and is antagonized by HIV-1 Vpu. Nature 451, 425-430.
94. Newman, R. M., Hall, L., Connole, M., Chen, G. L., Sato, S., Yuste, E., Diehl, W., Hunter, E., Kaur, A., Miller, G. M., and Johnson, W E. (2006). Balancing selection and the evolution of functional polymorphism in Old World monkey TRIM5alpha. Proc. Natl. Acad. Sci. U.S.A. 103, 19134-19139.
95. Newman, R. M., Hall, L., Kirmaier, A., Pozzi, L. A., Pery, E., Farzan, M., O'Neil, S. P., and Johnson, W (2008). Evolution of a TRIM5-CypA splice isoform in old world monkeys. PLoS Pathog. 4, e1000003. doi:10.1371/journal.ppat.1000003
96. Newstein, M., Stanbridge, E. J., Casey, G., and Shank, P. R. (1990). Human chromosome 12 encodes a species-specific factor which increases human immunodeficiency virus type 1 tat-mediated trans activation in rodent cells. J. Virol. 64, 4565-4567.
97. Nisole, S., Lynch, C., Stoye, J. P., and Yap, M. W. (2004). A Trim5-cyclophilin A fusion protein found in owl monkey kidney cells can restrict HIV-1. Proc. Natl. Acad. Sci. U.S.A. 101, 13324-13328.
98. Ohkura, S., Yap, M. W., Sheldon, T., and Stoye, J. P. (2006). All three variable regions of the TRIM5alpha B30.2 domain can contribute to the specificity of retrovirus restriction.J. Virol. 80, 8554-8565.
99. Pacheco, B., Finzi, A., Stremlau, M., and Sodroski, J. (2010). Adaptation of HIV-1 to cells expressing rhesus monkey TRIM5alpha. Virology 408, 204-212.
100. Perez-Caballero, D., Hatziioannou, T., Yang, A., Cowan, S., and Bieniasz, P. D. (2005). Human tripartite motif 5alpha domains responsible for retrovirus restriction activity and specificity. J. Virol. 79, 8969-8978.
101. Perron, M. J., Stremlau, M., and Sodroski, J. (2006). Two surface-exposed elements of theB30.2/SPRY domain as potency determinants of N-tropic murine leukemia virus restriction by human TRIM5alpha. J. Virol. 80, 5631-5636.
102. Price, A. J., Marzetta, F., Lammers, M., Ylinen, L. M., Schaller, T., Wilson, S. J., Towers, G. J., and James, L. C. (2009). Active site remodeling switches HIV specificity of antiretroviral TRIMCyp. Nat. Struct. Mol. Biol. 16, 1036-1042.
103. Reymond, A., Meroni, G., Fantozzi, A., Merla, G., Cairo, S., Luzi, L., Rig-anelli, D., Zanaria, E., Messali, S., Cainarca, S., Guffanti, A., Minucci, S., Pelicci, P. G., and Ballabio, A. (2001). The tripartite motif family identifies cell compartments. EMBO J.20,2140-2151.
104. Reynolds, M. R., Sacha, J. B., Weiler, A. M., Borchardt, G. J., Glidden, C. E., Sheppard, N. C., Norante, F. A., Castrovinci, P. A., Harris, J. J., Robertson, H. T., Friedrich, T. C., Mcdermott, A. B., Wilson, N. A., Allison, D. B., Koff, W. C., Johnson, W. E., and Watkins, D. I. (2011). The TRIM5{alpha} genotype of rhesus macaques affects acquisition of simian immunodeficiency virus SIVsmE660 infection after repeated limiting-dose intrarectal challenge. J. Virol. 85, 9637-9640.
105. Saito, A., Kono, K., Nomaguchi, M., Yasutomi, Y., Adachi, A., Shioda, T., Akari, H., and Nakayama, E. E. (2011a). Geographic, genetic and functional diversity of anti retroviral host factor TRIMCyp in cynomolgus macaque (Macaca fascicularis). J. Gen. Virol. doi: 10.1099/vir.0.038075-0. [Epub ahead of print].
106. Saito, A., Nomaguchi, M., Iijima, S., Kuroishi, A., Yoshida, T., Lee, Y J., Hayakawa, T., Kono, K., Nakayama, E. E., Shioda, T., Yasutomi, Y., Adachi, A., Matano, T., and Akari, H. (2011b). Improved capacity of a monkey-tropic HIV-1 derivative to replicate in cynomolgus monkeys with minimal modifications. Microbes Infect. 13, 58-64.
107. Sawada, S., Gowrishankar, K., Kitamura, R., Suzuki, M., Suzuki, G., Tahara, S., and Koito, A. (1998). Disturbed CD4+ T cell homeostasis and in vitro HIV-1 susceptibility in transgenic mice expressing T cell line-tropic HIV-1 receptors. J. Exp. Med. 187,1439-1449.
108. Sawyer, S. L., Wu, L. I., Emerman, M., and Malik, H. S. (2005). Positive selection of primate TRIM5alpha identifies a critical species-specific retroviral restriction domain. Proc. Natl. Acad. Sci. U.S.A. 102, 2832-2837.
109. Sayah, D. M., Sokolskaja, E., Berthoux, L., and Luban, J. (2004). Cyclophilin A retrotransposition into TRIM5 explains owl monkey resistance to HIV-1. Nature 430, 569-573.
110. Sebastian, S., and Luban, J. (2005). TRIM5alpha selectively binds a restriction-sensitive retroviral cap-sid. Retrovirology 2, 40.
111. Sheehy, A. M., Gaddis, N. C., Choi, J. D., and Malim, M. H. (2002). Isolation of a human gene that inhibits HIV-1 infection and is suppressed by the viral Vif protein. Nature 418, 646-650.
112. Sheehy, A. M., Gaddis, N. C., and Malim, M. H. (2003). The antiretroviral enzyme APOBEC3G is degraded by the proteasome in response to HIV-1 Vif. Nat. Med. 9,1404-1407.
113. Shibata, R., Sakai, H., Kawamura, M., Tokunaga, K., and Adachi,A. (1995). Early replication block of human immunodeficiency virus type 1 in monkey cells.J. Gen. Virol. 76(Pt 11), 2723-2730.
114. Song, B., Gold, B., O'Huigin, C., Javan-bakht, H., Li, X., Stremlau, M., Win-kler, C., Dean, M., and Sodroski, J. (2005a). The B30.2(SPRY) domain of the retroviral restriction factor TRIM5alpha exhibits lineage-specific length and sequence variation in primates. J. Virol. 79, 6111-6121.
115. Song, B., Javanbakht, H., Perron, M., Park, D. H., Stremlau, M., and Sodroski, J. (2005b). Retrovirus restriction by TRIM5alpha variants from old world and new world primates. J. Virol. 79, 3930-3937.
116. Song, H., Nakayama, E. E., Yokoyama, M., Sato, H., Levy, J. A., and Shioda, T. (2007). A single amino acid of the human immunodeficiency virus type 2 capsid affects its replication in the presence of cynomolgus monkey and human TRIM5alphas. J. Virol. 81,7280-7285.
117. Staal, F. J., Roederer, M., and Herzen-berg, L. A. (1990). Intracellular thiols regulate activation of nuclear factor kappa B and transcription of human immunodeficiency virus. Proc. Natl Acad. Sci. U.S.A. 87, 9943-9947.
118. Stremlau, M., Owens, C. M., Perron, M. J., Kiessling, M., Autissier, P., and Sodroski, J. (2004). The cytoplasmic body component TRIM5alpha restricts HIV-1 infection in old world monkeys. Nature 427, 848-853.
119. Stremlau, M., Perron, M., Lee, M., Li, Y., Song, B., Javanbakht, H., Diaz-Griffero, F., Anderson, D. J., Sundquist, W. I., and Sodroski, J. (2006). Specific recognition and accelerated uncoating of retroviral capsids by the TRIM5alpha restriction factor. Proc. Natl Acad. Sci. U.S.A. 103,5514-5519.
120. Stremlau, M., Perron, M., Welikala, S., and Sodroski, J. (2005). Species-specific variation in the B30.2(SPRY) domain of TRIM5alpha determines the potency of human immunodeficiency virus restriction. J. Virol. 79, 3139-3145.
121. Towers, G. J., Hatziioannou, T., Cowan, S., Goff, S. P., Luban, J., and Bieniasz, P. D. (2003). Cyclophilin A modulates the sensitivity of HIV-1 to host restriction factors. Nat. Med. 9, 1138-1143.
122. Van Damme, N., Goff, D., Katsura, C., Jorgenson, R. L., Mitchell, R., Johnson, M. C., Stephens, E. B., and Guatelli, J. (2008). The interferon-induced protein BST-2 restricts HIV-1 release and is downregulated from the cell surface by the viral Vpu protein. Cell Host Microbe 3, 245-252.
123. VandeWoude, S., and Apetrei, C. (2006). Going wild: lessons from naturally occurring T-lymphotropic lentiviruses. Clin. Microbiol Rev. 19, 728-762.
124. Virgen, C. A., Kratovac, Z., Bieniasz, P. D., and Hatziioannou, T. (2008). Independent genesis of chimeric TRIM5-cyclophilin proteins in two primate species. Proc. Natl. Acad. Sci. U.S.A. 105, 3563-3568.
125. Wei, P., Garber, M. E., Fang, S. M., Fischer, W. H., and Jones, K. A. (1998). A novel CDK9-associated C-type cyclin interacts directly with HIV-1 Tat and mediates its high-affinity, loop-specific binding to TAR RNA. Cell 92, 451-462.
126. Wilson, S. J., Webb, B. L., Maplanka, C., Newman, R. M., Verschoor, E. J., Heeney, J. L., and Towers, G. J. (2008a). Rhesus macaque TRIM5 alleles have divergent antiretroviral specificities. J. Virol. 82, 7243-7247.
127. Wilson, S. J., Webb, B. L., Ylinen, L. M., Verschoor, E., Heeney, J. L., and Towers, G. J. (2008b). Independent evolution of an antiviral TRIMCyp in rhesus macaques. Proc. Natl. Acad. Sci. U.S.A. 105, 3557-3562.
128. Wu, X., Anderson, J. L., Campbell, E. M., Joseph, A. M., and Hope, T. J. (2006). Proteasome inhibitors uncouple rhesus TRIM5alpha restriction of HIV-1 reverse transcription and infection. Proc. Natl. Acad. Sci. U.S.A. 103, 7465-7470.
129. Yap, M. W., Nisole, S., and Stoye, J. P. (2005). A single amino acid change in the SPRY domain of human Trim5alpha leads to HIV-1 restriction. Curr.Biol. 15,73-78.
130. Yeh, W W., Rao, S. S., Lim, S. Y., Zhang, J., Hraber, P. T., Brassard, L. M., Luedemann, C., Todd, J. P., Dod-son, A., Shen, L., Buzby, A. P., Whitney, J. B., Korber, B. T., Nabel, G. J., Mascola, J. R., and Letvin, N. L. (2011). The TRIM5 gene modulates penile mucosal acquisition of simian immunodeficiency virus in rhesus monkeys. J. Virol. 85, 10389-10398.
131. Ylinen, L. M., Keckesova, Z., Wilson, S. J., Ranasinghe, S., and Towers, G. J. (2005). Differential restriction of human immunodeficiency virus type 2 and simian immunodeficiency virus SIVmac by TRIM5alpha alleles. J. Virol. 79, 11580-11587.
132. Ylinen, L. M., Price, A. J., Rasaiyaah, J., Hue, S., Rose, N. J., Marzetta, E, James, L. C., and Towers, G. J. (2010). Conformational adaptation of Asian macaque TRIMCyp directs lineage specific antiviral activity. PLoS Pathog. 6, e1001062. doi:10.1371/journal.ppat. 1001062
133. Zhang, F., Wilson, S. J., Landford, W. C., Virgen, B., Gregory, D., Johnson, M. C., Munch, J., Kirchhoff, F., Bieniasz, P. D., and Hatziioannou, T. (2009). Nef proteins from simian immunodeficiency viruses are teth-erin antagonists. CellHostMicrobe 6, 54-67.
134. Zhao, G., Ke, D., Vu, T., Ahn, J., Shah, V B., Yang, R., Aiken, C., Charlton, L. M., Gronenborn, A. M., and Zhang, P. (2011). Rhesus TRIM5alpha disrupts the HIV-1 capsid at the inter-hexamer interfaces. PLoS Pathog. 7, e1002009. doi:10.1371/journal.ppat.1002009
135. Zheng, Y. H., Yu, H. F., and Peterlin, B. M. (2003). Human p32 protein relieves a post-transcriptional block to HIV replication in murine cells. Nat. CellBiol. 5, 611-618.